MPMI Vol. 26, No. 8, 2013, pp. 835–843. http://dx.doi.org/10.1094/MPMI-10-12-0249-CR.
e -Xtra*
CURRENT REVIEW
Sniffing on Microbes: Diverse Roles of Microbial Volatile Organic Compounds in Plant Health Vasileios Bitas,1 Hye-Seon Kim,2 Joan W. Bennett,3 and Seogchan Kang1 1
Department of Plant Pathology & Environmental Microbiology, The Pennsylvania State University, University Park 16802, U.S.A.; 2Department of Biological Sciences, University of Delaware, Newark 19711, U.S.A.; 3Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ 08901, U.S.A. Submitted 18 October 2012. Accepted 3 April 2013.
Secreted proteins and metabolites play diverse and critical roles in organismal and organism–environment interactions. Volatile organic compounds (VOC) can travel far from the point of production through the atmosphere, porous soils, and liquid, making them ideal info-chemicals for mediating both short- and long-distance intercellular and organismal interactions. Critical ecological roles for animal- and plant-derived VOC in directing animal behaviors and for VOC as a language for plant-to-plant communication and regulators of various physiological processes have been well documented. Similarly, microbial VOC appear to be involved in antagonism, mutualism, intra- and interspecies regulation of cellular and developmental processes, and modification of their surrounding environments. However, the available knowledge of how microbial VOC affect other organisms is very limited. Evidence supporting diverse roles of microbial VOC with the focus on their impact on plant health is reviewed here. Given the vast diversity of microbes in nature and the critical importance of microbial communities associated with plants for their ecology and fitness, systematic exploration of microbial VOC and characterization of their biological functions and ecological roles will likely uncover novel mechanisms for controlling diverse biological processes critical to plant health and will also offer tangible practical benefits in addressing agricultural and environmental problems. Every organism employs a network of signaling pathways to sense the environment and other organisms and to launch one or more specific molecular, cellular, or developmental changes. This signaling mechanism ensures cellular homeostasis, directs orderly growth and development, and controls behavior. Because sensing of the environment and other organism occurs often through the recognition of specific molecules, a vast array of secreted proteins and metabolites play key roles in these mechanisms. In turn, many organisms also have evolved the ability to exploit these mechanisms in other organisms to benefit themselves or coordinate symbiosis (Bednarek et al. 2010; Corresponding author: S. Kang; E-mail:
[email protected]; Telephone: +1.814.863.3846; Fax: +1.814.863.7217. * The e-Xtra logo stands for “electronic extra” and indicates that Figure 1 appears in color online. © 2013 The American Phytopathological Society
Bonfante and Anca 2009). The following examples illustrate the critical significance of secreted molecules for the health and fitness of plants: i) manipulation of physical and chemical properties of soil (e.g., organic acids to facilitate phosphorus acquisition and to chelate toxic heavy metals) and ii) control of interspecies interactions (e.g., allelopathy; volatile compounds to attract pollinators, seed dispersers, and parasitoids of herbivorous insects; antimicrobial compounds and proteins for defense; flavonoids to initiate the formation of symbiosomes by rhizobia; and strigolactones for mycorrhizal symbiosis). Plant-associated microbes also secrete various molecules that affect plant health both directly and indirectly (Bednarek et al. 2010; Bonfante and Anca 2009): i) altering physical and chemical properties of their immediate surroundings to increase nutrient availability for themselves and associated plants (e.g., siderophores for iron acquisition and enzymes and metabolites to facilitate phosphorus acquisition), ii) antagonizing pathogenic organisms (e.g., antibiotics and antimicrobial proteins), and iii) priming host cells for subsequent colonization (e.g., modulation of external pH to facilitate pathogenesis and molecules that coordinate symbiosis or quorum sensing). Pathogenic microbes secrete assorted virulence factors (or effectors) into plant–pathogen interspaces and the cytoplasm of host cells via specialized secretion systems, in order to attenuate host defense responses and support pathogen proliferation (Martin and Kamoun 2012). Plants have evolved to recognize certain pathogen-derived molecules as signals in the species- or isolate-specific (e.g., avirulence factors) and non-species-specific (e.g., fungal cell wall components and bacterial flagella and lipopolysaccharides) manners in order to initiate rapid and strong defense responses (Thomma et al. 2011). Collectively, molecules secreted by plants and microbes affect the structure and emergent properties of plant-associated microbial communities as well as the health of plants and soils (Bednarek et al. 2010; Berendsen et al. 2012; Lundberg et al. 2012). Organisms ranging from microbes to animals to plants secrete volatile organic compounds (VOC) that affect their environments and each other (Fig. 1) (Baldwin 2010; Effmert et al. 2012; Herrmann 2010; Kramer and Abraham 2012; Morath et al. 2012; Schulz and Dickschat 2007). Biogenic VOC exhibit certain common chemical and physical properties: they i) belong to chemical classes such as alcohols, thiols, aldehydes, esters, terpenoids, and fatty acid derivatives; ii) are usually lipophilic; and iii) have low molecular weight (100 plant species, and can also be
saprophytic. A nonpathogenic strain of F. oxysporum, MSA35, protects plants from pathogenic F. oxysporum isolates and is associated with a group of ectosymbiotic bacterial species (Minerdi et al. 2009, 2011). This strain enhanced the growth of lettuce via VOC production (Minerdi et al. 2011). When its symbiotic bacteria had been cured by serially culturing MSA35 in a medium amended with antibiotics, the cured strain could no longer promote plant growth (Minerdi et al. 2011). Comparison of VOC produced by MSA35 and the cured strain showed a difference in the production of some sesquiterpenes (Minerdi et al. 2009). Lettuce seedlings treated with β-caryophyllene (Fig. 2), one of the sesquiterpenes produced by MSA35, displayed phenotypes similar to those exposed to VOC from MSA35 (Minerdi et al. 2011). In contrast, VOC produced by fruiting bodies of the ectomycorrhizal truffles Tuber borchii, T. indicum, and T. melanopsorum inhibited root development and foliar growth of Arabidopsis thaliana and their host Cistus incanus and, in some cases, caused phytotoxicity (Splivallo et al. 2007). When 10 main truffle VOC tested individually, most of them negatively affected the seed germination, primary root elongation, and leaf growth of A. thaliana. In-depth analyses with two VOC, 1-octen-3-ol and trans2-octenal, suggested that modification of the oxidative metabolism by these VOC might underlie the negative effects on growth (Splivallo et al. 2007). Given the vast diversity of microbes in and around plants, the number of bacterial and fungal species that have been analyzed for the production of VOC that affect plants is grossly inadequate. Furthermore, the focus of most previous surveys has been on those dwelling in soils, especially the rhizosphere. A systematic survey of microbial communities associated with diverse plants in different ecosystems, including those associated with aboveground parts of plant (e.g., endophytes and phyllosphere microbes), is needed to advance our understanding of the evolution and roles of microbial VOC in modulating plant growth and fitness. Microbial VOC as chemical weapons against other microbes. Most microbes reside in their ecological niches in close association with other organisms. The structure and emergent properties of such communities are intimately linked to how their members interact with each other and the environment (Konopka 2009). Competition for nutrients and space probably is the most common form of interaction and often leads to a chemical warfare, in which competing members secrete a diverse array of proteins and compounds to suppress or kill the others. Some bacteria and fungi that are well equipped with such weapons have been exploited as biocontrol agents to manage plant pathogens (Pal and McSpadden Gardener 2007). A main motivation that has driven studies on antimicrobial VOC is the potential utility of VOC and their producers as novel agents for pathogen control. Synthetic and plant-derived VOC already have been extensively utilized to manage insect pests (Thacker and Train 2010). However, although the exploration of antimicrobial VOC started decades ago (McCain 1966), this field still is in its infancy because most studies have focused on discovery, with little known about how antimicrobial VOC affect target microbes. VOC produced by several bacteria have been shown to inhibit spore germination and mycelial growth or cause abnormal morphological changes in fungi (Effmert et al. 2012). Among 197 bacterial strains cultured from canola and soybean plants, 14 of them, most of which belong to four Pseudomonas spp., consistently produced VOC that inhibited germination of sclerotia and ascospores or mycelial growth of Sclerotinia sclerotiorum, a major fungal pathogen of these plants, in vitro
and in soil tests (Fernando et al. 2005). Among the 23 volatiles from these isolates, benzothiazole, cyclohexanol, n-decanal, dimethyltrisulfide, 2-ethyl-1-hexanol, and nonanal (Fig. 2) completely inhibited mycelial growth and sclerotial germination. None of the 14 isolates produced all six compounds, indicating that different strains produce different combinations of common and strain- or species-specific antifungal volatiles. A more extensive survey involving 1,018 bacterial isolates showed that VOC from 328 isolates, which belong to families Alcaligenaceae, Bacillales, Micrococcaceae, Rhizobiaceae, and Xanthomonadaceae, inhibited spore germination and mycelial growth of two nematicidal fungi (Zou et al. 2007). Seven VOC, including acetamide, benzaldehyde, benzothiazole, 1butanamine, methanamine, phenylacetaldehyde, and 1-decene, appear to play roles in fungistasis. Benzothiazole was the only VOC that was found in both surveys, suggesting that different species produce different VOC for fungistasis, antifungal activity of many compounds are target specific, or a combination of both. Although alterations in enzyme activities or gene expression in fungi have been observed upon exposure to certain bacterial VOC in several studies (Effmert et al. 2012), the question of what molecular changes underpin fungistasis has not been clearly answered. Not surprisingly, fungi also produce VOC exhibiting antibacterial or anti-fungal activity. Some of the VOC produced by the oyster mushroom Pleurotus ostreatus inhibited the growth of several bacterial species at concentrations found in its fruit body (Beltran-Garcia et al. 1997). Fungal endophytes confer multiple fitness benefits, including enhanced resistance to biotic and abiotic stresses (Porras-Alfaro and Bayman 2011), but the underlying mechanisms are poorly understood. Certain endophytes produce antimicrobial VOC which may directly contribute to defense against pathogens. Chokol K, a VOC produced by the grass endophyte Epichloë sp., inhibited the growth and spore germination of two mycoparasites associated with stromata, the fruiting structure of Epichloë spp., and two plant-pathogenic fungi (Steinebrunner et al. 2008a). Muscodor albus, a fungal endophyte originally isolated from cinnamon tree, emits a mixture of VOC that inhibit or kill a broad range of bacteria, fungi, and oomycetes (Strobel et al. 2001). Analysis of its VOC via GC-MS and bioassays with identified compounds led to the identification of many antimicrobial VOC, with 1-butanol and 3-methyl-acetate being most effective (Strobel 2006a; Strobel et al. 2001). However, none was lethal to the testers individually, suggesting that Muscodor VOC work synergistically or additively (Strobel, 2006a). Additional M. albus isolates and related species, some of which exhibit similar VOC-mediated antimicrobial activities, have been isolated (Strobel 2006b; Zhang et al. 2010). The potential of M. albus and its VOC as biofumigants for controlling plant pathogens, human pathogens, and post-harvest pathogens has been demonstrated (Mercier and Smilanick 2005; Ramin et al. 2005; Strobel et al. 2001). Some biocontrol fungi appear to employ VOC to control pathogenic fungi (Bruce et al. 2003; Humphris et al. 2002; Hynes et al. 2007). Members of the genus Trichoderma have been shown to effectively parasitize or inhibit a wide range of soilborne fungal pathogens by employing multiple mechanisms, such as mycoparasitism, nutrient competition, and secretion of inhibitory compounds and hydrolytic enzymes (Harman 2011; Lorito et al. 2010). Trichoderma viride and T. aureoviride emitted VOC that inhibit the growth and protein production of Serpula lacrymans, a wood-rotting basidiomycete. However, T. pseudokoningii had no effect on any of the Serpula isolates tested, suggesting the species-specific nature of antifungal VOC production (Humphris et al. 2002). Similarly, the degree of growth inhibition of F. oxysporum f. sp. ciceris, a Vol. 26, No. 8, 2013 / 839
soilborne fungal pathogen that causes chickpea wilt, by VOC produced by multiple isolates of three Trichoderma spp. also varied depending on the combination of the Trichoderma and F. oxysporum f. sp. ciceris isolates tested (Dubey et al. 2007). F. oxysporum strain MSA35, which enhanced lettuce growth via VOC (Minerdi et al. 2011), also produces VOC that inhibit the growth of pathogenic strains of F. oxysporum, and the production of these antifungal VOC requires the presence of ectosymbiotic bacteria (Minerdi et al. 2009). Although the VOC contributing to Trichoderma spp.’s biocontrol activity have not yet been identified, α-humulene (Fig. 2), a sesquiterpene emitted by MSA35, but not MSA35 cured of its symbiotic bacteria, was shown to inhibit mycelial growth and downregulate the expression of several virulence genes in pathogenic F. oxysporum strains, supporting its involvement in biocontrol (Minerdi et al. 2009). Fungal VOC as signals mediating intra- and interspecies communications. Some microbial VOC are utilized for dialog rather than warfare. Just as bacteria coordinate their activities in their communities via chemical signals (e.g., quorum sensing via the use of N-acyl homeserine lactone), fungi also use diverse chemical signals, some of which are volatile, to control processes critical to their ecology and reproduction such as nutrient acquisition, sporulation, spore germination, and sexual development (Bennett et al. 2013; Leeder et al. 2011). Accordingly, VOC that affect such processes control the structure and emergent properties of the microbial communities associated with plants, thus influencing the plant health and fitness both directly and indirectly. One well-known form of communication occurs when too many spores exist in proximity. Under such conditions, fungi suppress spore germination through the use of self-inhibitors (a phenomenon known as the “crowding effect”), probably to enhance the likelihood of survival and proliferation upon germination. Penicillium paneum employs 1-octen-3-ol (Fig. 2), a VOC commonly produced by many other fungi, to control conidial germination in a reversible manner (Chitarra et al. 2004, 2005). This VOC was shown to inhibit germ-tube formation, alter the intracellular pH, increase the permeability of the membrane, and alter protein expression (Chitarra et al. 2005). In Trichoderma spp., 1-octen-3-ol and its analogs 3-octanol and 3-octanone (Fig. 2) appear to participate in controlling conidiation in a concentration-dependent manner (Nemcovic et al. 2008). Conidiating colonies of Trichoderma spp. produced these VOC and induced conidiation in neighboring colonies even in the absence of light, a known inducer of conidiation, suggesting that certain VOC may act as fungal “hormones” and control fungal development (Leeder et al. 2011). Many fungi rely on insects for dispersing their spores, a service critical for secondary colonization, disease development, and sexual development, and some of these fungi produce VOC mimicking those produced by flowers to attract pollinator insects (Bruce et al. 2005; Dudareva et al. 2006; Roy 1993). This mimicry also works in the opposite direction, because certain flowering plants produce VOC that mimic the scent of mushroom fruiting bodies to attract insects (Kaiser 2006). The heterothallic mating system of the grass endophytic Epichloë sp. relies on Botanophila flies for transferring gametic spores from grasses colonized by strains of the opposite mating type to stromata. Analysis of VOC produced by stromata of five Epichloë spp. and field bioassays using synthetic compounds led to the identification of two compounds, methyl (Z)-3-methyldodec-2-enoate (Steinebrunner et al. 2008b) and chokol K (Schiestl et al. 2006; Steinebrunner et al. 2008b) as major attractants. Both compounds elicit re840 / Molecular Plant-Microbe Interactions
sponses in the fly olfactory system (Steinebrunner et al. 2008b). Other fungal VOC, such as 1-3-octanol, 1-octen-3-ol, and octan-1-ol (Fig. 2), also have been shown to attract insects (Faldt et al. 1999). Synthesis: biological and ecological roles of microbial VOC represent a mostly uncharted frontier that awaits systematic explorations. Given the large number of VOC identified from the limited number of microbial species surveyed to date (Effmert et al. 2012; Kramer and Abraham 2012; Schulz and Dickschat 2007), we have observed only a glimpse of this chemical ecology frontier. Not only are many novel VOC and their functions waiting to be discovered but known VOC also are likely to have hitherto unrecognized biological and ecological roles, some of which may offer novel solutions for managing agricultural and environmental problems. Systematic exploration of microbes in diverse ecosystems, in combination with their phylogenetic contexts, will help us to develop hypotheses concerning the evolution, function, and ecological roles of VOC production in microbes. Microbial culture collections, especially those associated with detailed genotypic and phenotypic data, offer readily available materials for comprehensive survey of VOC in specific taxa. Resulting data not only will advance our understanding of critical ecosystem processes and services but also will assist in developing novel means for controlling agricultural and environmental problems via the use of beneficial microbes. Multiple indicators that are associated with the composition and activity of microbial communities have been employed to study how these communities impact ecosystems and how changing environmental conditions or human activities have impacted them. McNeal and Herbert (2009) proposed the utility of VOC as potential indicators to assess the status of soil microbial communities over large spatiotemporal dynamics and environmental perturbations (McNeal and Herbert 2009). As our understanding of how various microbial VOC affect ecosystems and their constituents increases, the accuracy and value of VOC profiles as such indicators will likely improve. Versatile application of plant-derived VOC such as neem oil and Chrysanthemum monoterpenes in controlling pests is well established (Thacker and Train 2010). Metabolic engineering of plants or plant-associated microbes to produce VOC with fumigant activity may work as an alternative to traditional chemical control of pests. Microbial VOC-mediated growth promotion and stress resistance in plants (Farag et al. 2006; Gutierrez-Luna et al. 2010; Han et al. 2006; Kwon et al. 2010; Minerdi et al. 2009; Ryu et al. 2003, 2004; Zhang et al. 2008a,b) suggest that certain microbes and their VOC could be deployed to alleviate the heavy dependence of crop production on chemical input. The short-lived “pesticide revolution,” caused by the rapid selection and spread of pesticide-resistant insects, and the emergence of resistance to chemicals that control weeds and microbial pathogens has created a boom-andbust cycle (Lewis et al. 1997). Plant breeding programs for disease resistance and chemical controls mostly neglect microbial partners and unknowingly may destroy this critical partnership. In order to feed the increasing world population without severely degrading the environment, we need to explore alternative or complementary solutions to current practices. Restoring or fortifying key plant–microbe partnerships would make crop plants rely less on human intervention; this strategy is particularly critical for resource-limited subsistence farming. Several major pitfalls and challenges face researchers who seek to illuminate the roles and potential applications of microbial VOC. VOC-producing organisms emit many different compounds simultaneously, and the composition of produced VOC
is highly dynamic and likely influenced by multiple factors, such as nutrient and oxygen availability and the physiological state of the VOC producer (Insam and Seewald 2010). Accordingly, phenotypes in a tester organism may vary depending on how bacteria or fungi are cultured. Furthermore, individual VOC are likely to work synergistically or antagonistically with other VOC to affect target organisms, suggesting that, under certain experimental conditions, VOC that cause opposite effects may cancel out each other’s effect and fail to cause notable phenotypes. Although evaluating identified VOC individually using their synthetic versions is a potential solution, this approach may miss VOC combinations that work synergistically. Although it probably is not practical to employ experimental designs that address all these potential pitfalls, employment of multiple well-controlled experimental conditions is critical in order not to miss too many potentially important VOC and their biological effects. Two studies (Blom et al. 2011a; Kai and Piechulla 2009) further underscored the importance of proper experimental design and appropriate controls to accurately evaluate the role of microbial VOC in modulating plant growth and other important traits. Because increased CO2 resulting from microbial catabolism in a closed assay system such as the I plate will enhance plant growth, negative effects of certain VOC may be masked and the degree of growth enhancement by other VOC will likely be inflated (Kai and Piechulla 2009). A survey of soil bacteria for their ability to affect the growth of A. thaliana revealed the critical importance of culture conditions in their VOC production (Blom et al. 2011a). Depending on the culture medium used and the inoculum density, the same strains caused opposite effects on the plants exposed to their VOC ranging from death to sixfold increase in biomass, suggesting that culture conditions significantly modulated their VOC profiles, including the type and amount of compounds (Blom et al. 2011a). This study underscores the importance of studying potential roles of microbial VOC in consideration of factors that can potentially affect VOC production. In nature, organisms near and far are potential targets for microbial VOC, and the same VOC may perform disparate functions in many different organisms, making it difficult to choose appropriate target organisms and assay conditions for uncovering functions. However, potential clues can be found in known biological traits and ecological niches of individual microbial species and their relatives, because it is likely that the production of specific VOC is linked to the biology and ecology of individual species. For example, in discovering functions for VOC commonly produced by microbes that are closely associated with specific plants, obvious targets for evaluating their functions are host plants and other organisms associated with the host plants. The multifaceted effects of individual VOC compounds and their differential functions, depending on environmental factors and target organisms, also potentially complicate the elucidation of their roles. A good example is the common fungal volatile 1-octen-3-ol, which has been shown to affect insects (Faldt et al. 1999), plants (Kishimoto et al. 2007), and fungi (Chitarra et al. 2004). When scientists within a given subdiscipline focus on a narrow set of observable changes and potential targets, we run the risk of failing to recognize important roles and can potentially skew our view on VOC functions. Despite these challenges, microbial VOC-mediated signaling is a potential gold mine we should explore. Model microbes and plants with rich resources and accumulated knowledge will help overcome some of the experimental challenges. As reviewed above, studies in the model plant A. thaliana have been instrumental in elucidating the function and mechanism of action of VOC from both bacteria and fungi. This model
plant will continue to facilitate systematic screening of diverse microbes for their ability to affect plants via VOC production and subsequent studies on underlying mechanisms, thus serving as a stepping stone for parallel studies on economically important plants. However, because A. thaliana may not respond to certain VOC that otherwise affect other plants, the importance of developing additional model plants cannot be overlooked. Another key consideration is balancing laboratory and field studies. Technological advances with respect to profiling and analyzing VOC; genome sequencing and functional genomics tools; and tools for studying the molecular, physiological, and cellular changes in plant and microbial systems no doubt will accelerate studies on the biosynthesis and modes of action of microbial VOC. Finally, we must remember that, despite their enormous reductionist value, such molecular approaches cannot substitute for field experiments that evaluate the roles of VOC and their producers under natural ecological settings. Advancement of our fundamental understanding as well as the development and deployment of VOC-based solutions for agricultural and environmental problems will require approaches at many levels. ACKNOWLEDGMENTS We thank the Penn State College of Agricultural Sciences and Rutgers University for their support; D. Whalen, J. Demers, and N. Naranjo for help with manuscript preparation; R. Hung and S. Lee for providing useful input to our thinking about the ecological roles of fungal VOC; and three anonymous reviewers and the editor of this review for their critical suggestions and instrumental help in improving this review.
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